Review on the effects of exposure to spilled oils on human health.

Abstract

Harmful effects of oil spills on diverse flora and fauna species have been extensively studied. Nevertheless, only a few studies have been compiled in the literature dealing with the repercussions of oil exposure on human health; most of them have focused on acute effects and psychological symptoms. The objective of this work was to gather all these studies and to analyze the possible consequences of this kind of complex exposure in the different aspects of human health. Studies found on this topic were related to the disasters of the Exxon Valdez, Braer, Sea Empress, Nakhodka, Erika, Prestige and Tasman Spirit oil tankers. The majority of them were cross-sectional; many did not include control groups. Acute effects were evaluated taking into account vegetative-nervous symptoms, skin and mucous irritations, and also psychological effects. Genotoxic damage and endocrine alterations were assessed only in individuals exposed to oil from Prestige. The results of the reviewed articles clearly support the need for biomonitoring human populations exposed to spilled oils, especially those individuals involved in the cleanup, in order to evaluate not only the possible immediate consequences for their health but also the medium- and long-term effects, and the effectiveness of the protective devices used.

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Review on the effects of exposure to spilled
oils on human health
Francisco Aguilera,a,b,cJosefina Méndez,bEduardo Pásaroaand
Blanca Laffona*
ABSTRACT: Harmful effects of oil spills on diverse flora and fauna species have been extensively studied. Nevertheless, only a
fewstudieshavebeencompiledintheliteraturedealingwiththerepercussionsofoilexposureonhumanhealth;mostofthem
have focused on acute effects and psychological symptoms. The objective of this work was to gather all these studies and to
analyzethepossibleconsequencesofthiskindofcomplexexposureinthedifferentaspectsofhumanhealth. Studiesfoundon
this topic were related to the disasters of the Exxon Valdez, Braer, Sea Empress, Nakhodka, Erika, Prestige and Tasman Spirit oil
tankers. The majority of them were cross-sectional; many did not include control groups. Acute effects were evaluated taking
into account vegetative-nervous symptoms, skin and mucous irritations, and also psychological effects. Genotoxic damage
and endocrine alterations were assessed only in individuals exposed to oil from Prestige. The results of the reviewed articles
clearlysupporttheneedforbiomonitoringhumanpopulationsexposedtospilledoils,especiallythoseindividualsinvolvedin
the cleanup, in order to evaluate not only the possible immediate consequences for their health but also the medium- and
long-term effects, and the effectiveness of the protective devices used. Copyright © 2010 John Wiley & Sons, Ltd.
Keywords: acute toxicity; endocrine toxicity; epidemiological studies; genotoxic effects; human health; oil spills; psychological
effects
INTRODUCTION AND BACKGROUND
Since the industrial revolution took place in the eighteenth
century, the use of fossil fuels, especially petroleum derivatives,
hascontinuallyincreased.Itrequirestheirtransportfromtheplat-
forms where they are extracted around the world, usually along
sea routes in big tankers.The bad state of a considerable number
ofthese,addedtothefactthatmanyarestillmonohull,hasledto
the high number of accidental spills that have occurred in recent
decades.
In the last five decades approximately 38 accidents involving
supertankers have taken place, affecting the coasts of different
countries (International Tankers Owners Pollution Federation
Limited;http://www.itopf.com/information-services/data-and-
statistics/statistics/index.html#noha/). The major oil spills have
occurred in western and Mediterranean Europe, as well as in
North Africa; these regions have experienced 13 of the 20 major
spills. In this respect and considering the high population density
of these geographical areas, they have major interest from the
epidemiological point of view.
Themainecosystemconstituentsaffectedbythespillsaregen-
erally seaside flora and some fauna such as birds and bivalve
mollusks. Nevertheless, when a big spill occurs there is usually a
largegroupofvolunteers,ingenerallocalinhabitants,whomobi-
lize and take part in the cleanup work to minimize the impact of
the spill on the natural and economic resources and recover the
coastal environment as soon as possible. These individuals con-
stitute an exposed population whose health may be potentially
affected by the noxious properties of the oil.
Harmful effects of oil spills on diverse marine species, espe-
cially birds and marine invertebrates, have been extensively
studied. It is enough to type the name of any sunken oil tanker
(e.g. Exxon Valdez, Nakhodka, Erika, Urquiola, Braer, Sea Empress,
Prestige) into a bibliographic search engine (e.g. PubMed) and
many studies on the impact of the spill on coastal ecosystems
and the contamination and recovery are obtained. Nevertheless,
there are only a few studies focused on the repercussions of oil
exposure for human health. Most of them are related to acute
effects and psychological symptoms. Table 1 displays a summary
of the main characteristics of those oil spills for which epidemio-
logical studies on the effects on human health have appeared in
the literature.
The objective of this manuscript is to review the studies on the
effects of oil exposure on human health as a result of accidents
involving supertankers. Studies were classified according to the
type of effect analyzed into acute toxic and psychological effects
or genotoxic and endocrine effects; also a section compiling
some in vitro works and studies on the bioaccumulation
and transference of oil compounds in the food chain is
included.
*Correspondence to: B. Laffon, Toxicology Unit, University of A Coruña, Edificio de
Servicios Centrales de Investigación, Campus Elviña s/n, 15071-A Coruña, Spain.
E-mail: blaffon@udc.es
aUnidad de Toxicología, Dpto. Psicobiología, Universidad de A Coruña, España
bDpto. Biología Celular y Molecular, Universidad de A Coruña, España
cCarrera de Tecnología Médica, Facultad de Medicina, Universidad de Valparaíso,
Chile
Review
Received: 11 January 2010, Revised: 25 February 2010,Accepted: 26 February 2010 Published online in Wiley InterScience: 14 April 2010
(www.interscience.wiley.com) DOI 10.1002/jat.1521
291
J. Appl. Toxicol. 2010; 30: 291–301
Copyright © 2010 John Wiley & Sons, Ltd.

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IN VITRO STUDIES AND STUDIES ONTHE
EFFECTS CAUSED BY TRANSFERENCE TO THE
FOOD CHAIN
Table 2displaysasummaryofthestudiesincludedinthissection.
All of them analyzed effects induced by oil spilled from Erika.
Amat-Bronnert et al. (2007) performed an in vitro study in two
human cell lines, one from hepatoma and another one from
bronchial epithelium, treated with an Erika fuel extract. DNA
adducts performed by
detected in hepatoma cells, indicating biotransformation via
cytochrome P450 (CYP) 1A2 and 1B1 since the two cell lines do
notpossessthesamemetabolicsystem(hepatomacellsexhibita
wide spectrum of metabolic enzymes while bronchial cells do
not). Moreover, western blot and densitometry quantification
showed that exposure to the fuel extract induced some metabo-
lizing enzymes such as CYP 1A2, cyclooxygenase 2 and
5-lipooxygenase; the latter two are involved in carcinogenic pro-
cesses. In epithelial bronchial cells induction of leucotriene B4,
a mediator of inflammation, was revealed by inmmunoassay.
These results acquire special importance with regard to human
health, since inhalation is one of the most representative ways of
absorbing fuel compounds.
Lemiere et al. (2005) carried out a study to determine the
potential genotoxic risk for consumers of marine food contami-
nated with polycyclic aromatic hydrocarbons (PAH) coming
from oil spills. Mussels (Mytilus sp.) contaminated with Erika oil
were collected and provided daily to rats over periods of 2 and
4 weeks. The DNA damage was measured by the single-cell gel
electrophoresis (comet) assay in hepatic, bone marrow and
blood cells. While no evidence of genotoxicity was observed in
the peripheral blood samples, significant increases in DNA
damage were observed in the liver and the bone marrow of rats
(P < 0.001). The intensity of the DNA damage increased with the
PAH contamination level of the mussels. Therefore, this study
demonstrated that oil-contaminated food can cause genotoxic
damage in consumers. Also, it showed that mussels, often
present in the human diet especially in coastal producer
regions, carry pollutants in a bioavailable form when contami-
nated with oil.
A similar study in rats fed with Erika oil-contaminated
mussels(Mytilusedulis)wasperformedbyChatyet al.(2008).Rats
were fed for 2 days and CYP 1A1 mRNA expression and
ethoxyresorufin-O-deethylase (EROD) catalytic activity were ana-
lyzed by RT-PCR and a fluorimetric method, respectively. Results
obtained showed the transient induction of CYP 1A1 mRNA and
EROD activity, which reached a maximum after 12 h, returning to
basal levels within 36 h.
32P-postlabelling method were only
The studies presented in this section show evidence for the
bioaccumulation of oil compounds and their transference to
thefoodchaininoil-contaminatedmarinefood,anddemonstrate
the induction of DNA damage by the products generated by
metabolic enzyme activity transforming many polluting agents
intoevenmoretoxicintermediaries.Inthisregard,Bro-Rasmussen
(1996) indicated that toxic chemicals at low concentrations will
notimmediatelykillhumans;however,dependingontheirpoten-
tial to bioconcentrate when climbing the food chain, persistent
chemicals may create a human hazard in the case of chronic
ingestion.Forthisreason,invitroandinvivostudiesthatconsider
not only bioaccumulation ability, but also the time that the pol-
lutants stay in the organisms and the transference rate through
the different links of the food chain, must be performed, and also
studiesontheoptimalwaytodecontaminateoil-exposedorgan-
isms to make them safe for human consumption.
EPIDEMIOLOGICAL STUDIES ON ACUTE
TOXIC AND PSYCHOLOGICAL EFFECTS, AND
STUDIES ON POTENTIAL TOXICOLOGICAL
RISK ASSESSMENT
A summary of the studies included in this section is shown in
Table 3.
Exxon Valdez
Thefirstoilspillforwhichstudiesontheeffectsonhumanhealth
are collected in the literature is the one from Exxon Valdez.
Althoughavarietyofstudiesexistontheecologicalimpactofthis
spill, only a few consider the psychological, psychiatric and social
effects.
Palinkas et al. (1992) assessed the levels of depressive symp-
tomathology between two groups, one of indigenous people
(N = 188) and another one of Euro-Americans (N = 371), all of
them residents in 13 communities of Alaska (11 in the region
directly exposed to the oil spill itself and two control communi-
ties). The results of these authors suggested that cultural differ-
ences played an important role in the perception of the
psychological damage produced by this disaster, which was
related to the cleaning work in which the people were involved
and also the damage to fishing grounds, the main sustenance of
these communities. The group of Euro-Americans showed a
certain moderating effect of the damage in relation to familiar
support;however,thisfactordidnotsignificantlyinfluenceinthe
indigenous groups. These results emphasize the role of cultural
differences in the perception of and capacity to overcome the
psychological impact.
Table 1.
Oil spills for which epidemiological studies on the effects on human health were reported (ordered by spill size)
Ship nameDateLocation
Spill size (t)
MV Braer
Sea Empress
Prestige
ExxonValdez
Tasman Spirit
Erika
Nakhodka
5 January 1993
15 February 1996
19 November 2002
24 March 1989
26 July 2003
12 December 1999
2 January 1997
Southwest Shetland islands,UK
Milford Haven,UK
Galicia,Spain
Bligh ref,Prince William,Alaska,USA
Karachi,Pakistan
South Penmarch,Brittany,France
Northeast Oki Island,Sea of Japan,Japan
85,000
72,000
63,000
37,000
37,000
20,000
>6,000
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Later, the same authors (Palinkas et al., 1993) as a result of this
same disaster examined the relationship between exposure and
subsequent cleanup efforts and the prevalence of generalized
anxiety disorder, post-traumatic stress disorder (PTSD) and
depressive symptoms in 13 communities of Alaska. They per-
formed a community survey of 599 men and women approxi-
mately 1 year after the spill. Prevalences of 20.2 and 9.4% were
found for the generalized anxiety disorder and PTSD, respec-
tively. Also, the prevalence of depression scale scores above 16
and 18 was 16.6 and 14.2%, respectively. For all the parameters
analyzed, exposed individuals showed scores several times
higher than unexposed individualsWomen were particularly vul-
nerable to the effects of exposure to the oil spill and cleanup
activities on the prevalence of generalized anxiety disorder (b =
0.22, P < 0.0001; odds ratio = 1.43, 95% CI 1.23–1.67), PTSD (b =
0.19, P < 0.001; odds ratio = 1.40, 95% CI = 1.15–1.69) and CES-D
Scalescoresof18andabove(b=0.17,P<0.001;oddsratio=1.35,
95% CI = 1.13–1.60). The authors suggest, on the basis of their
results, improving the mental health care of disaster victims, par-
ticularly in primary care settings.
GillandPicou(1998)monitoredtheimpactofExxonValdezspill
on the affected populations by means of a 4-year (1989–1992)
longitudinal study in which they applied a survey on social dis-
ruption and psychological stress, using random-sampling strate-
gies, personal interviews and control communities. Data
obtained revealed the chronic nature of stress. Out-migration
expectations and desires increased from 1989 to 1991. Social
disruption was reported by a high proportion of residents in
1989, but had declined to just over half in 1991. High levels of
event-related psychological stress were found in 1989 and 1990
but they diminished in the following two years.
Finally, Palinkas et al. (2004) confirmed the prevalence of PTSD
associated with ethnic differences. They reported high levels of
social disruption one year after this disaster, in both ethnic
groups (indigenous Alaskan and Euro-Americans). However, low
level family support, participation in spill cleanup activities and a
decline in subsistence activities were significantly associated
with PTSD in indigenous Alaskan, but not in Euro-Americans.
MV Braer
Campbellet al.(1993)performedacross-sectionalstudyinwhich
a population of individuals exposed to MV Braer oil spill (N = 420)
was compared with a control group (N = 92), from Hillswick,
95 km north of the incident. They compiled information on
demographicdetails,smokingandalcoholconsumption,percep-
tion of health, peak expiratory flow, hematology, liver and renal
function tests, and blood and urine toxicology. Their results
showed that, during the first and second day after the spill, the
population reported mainly headaches, irritation of the throat
and itchy eyes. The authors did not find significant differences
between both groups for any of the biological markers. Taking
these results together, only anecdotal reports of certain acute
symptoms could be confirmed.
Later, the same authors reported longer-term effects in the
same populations (344 exposed individuals and 77 controls;
Campbell et al., 1994). Among exposed people, 7% perceived
their health to be poor compared with none of the controls (c2=
8.05, d.f. = 3, P < 0.05). Comparison of the symptoms of exposed
people in the 2 weeks before with their presence immediately
after the incident showed more tiredness and fever, and fewer
throat, skin and eye irritations, and headaches (odds ratio = 1.86,
Table 2.
In vitro studies and studies on the effects caused by transference to the food chain (in order of the chronology of the spills)
Accident –reference
Study characteristics
Methods
Results
Erika – Amat-Bronnert et al.(2007)
In vitro genotoxicity of an Erika fuel extract
in human epithelial bronchial cells and
human hepatoma cells
DNA adducts.
CYP 1A1,1A2,1B1,2C9,COX1,COX2 and
5-LOX protein expression.
LT B4 and PG E2 detection
Adducts formation and induction of CYP
1A2,COX2 and 5-LOX in hepatoma cells.
Formation of LT B4 in bronchial cells
Erika – Lemiere et al.(2005)
Genotoxicity associated with Erika
oil-contaminated mussels consumption
in rats fed daily for 2 and 4 weeks
Comet assay in hepatic cells,bone marrow
and blood cells
Dose–effect–time relationship in hepatic
and bone marrow cells.
No effect in blood cells
Erika – Chaty et al. (2008)
CYP 1A1 induction associated with Erika
oil-contaminated mussels consumption
in rats fed for 2 days
CYP 1A1 mRNA expression and EROD
catalytic activity in liver
CYP 1A1 mRNA and EROD activity
transient induction
COX, cyclooxygenase; CYP, cytochrome P450; EROD, ethoxyresorufin-O-de-ethylase; LOX, lipooxygenase; LT, leucotriene; PG, prostaglandine.
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Table 3.
Epidemiological studies on acute toxic and psychological effects, and studies on potential toxicological risk assessment (ordered by the chronology of the spills)
Accident – reference
Study characteristics
Methods
Results
Exxon Valdez –
Palinkas et al.(1992)
Cross-sectional.
Ethnic differences in stress,coping,and
depressive symptoms in indigenous people
(N = 188) and
Euro-Americans (N = 371)
CES-D scale
Level of exposure significantly associated with CES-D scores in both groups.
Indigenous people had significantly higher mean depressive symptom score.In Euro-Americans perceived family support was a moderator of effects of
exposure on depressive symptoms
Exxon Valdez –
Palinkas et al.(1993)
Cross-sectional,1 year after the spill.Community patterns of psychiatric-disorders in
exposed (N = 437) and controls (N = 162)
CES-D scale.
Questions from the National Institute of
Mental Health Diagnostic Interview
Schedule
The exposed group showed higher prevalence of generalized anxiety disorder
and CES-D scores ? 16 and 18.
Women exposed were particularly vulnerable
Exxon Valdez – Gill
and Picou (1998)
Longitudinal (4 years).
Chronic community stress and social effects in
residents:
1989 (N = 118)
1991 (N = 228)
1992 (N = 152)
and controls:
1989 (N = 73)
1991 (N = 102)
1992 (N = 41)
Questionnaires of out-migration desires,
expectations and social disruption.
Psychological stress by Events Scale
Data revealed the chronic nature of stress.
In residents increase in out-migration expectations and desires,and high levels
of event-related psychological stress,diminishing with time,was observed
Exxon Valdez –
Palinkas et al.(2004)
Cross-sectional,1 year after the spill.
Ethnic differences in symptoms of PTSD in
indigenous people (N = 188) and
Euro-Americans (N = 371)
Modified form of Version III of the DIS
High levels of social disruption were associated with PTSD in both ethnic
groups.
Low family support,participation in cleanup activities,and a decline in
subsistence activities were significantly associated with PTSD only in
indigenous people
MV Braer – Campbell
et al.(1993)
Cross-sectional.
Initial acute effects in residents (N = 420) and
controls (N = 92)
Questionnaires of acute symptoms,peak
expiratory flow,hematology,liver and renal
function tests,blood and urine toxicology
Principal health effects arose on days 1 and 2 (headaches,itchy eyes,and throat
irritation).
No significant differences between exposed and controls were found for any of
the biological markers.
Toxicological studies did not show any exposure that are known to affect
human health
MV Braer – Campbell
et al.(1994)
Cross-sectional.
Follow up after 6 months of acute effects in
residents (N = 344) and controls (N = 77)
General health questionnaire.
Peak expiratory flow,urine analysis,
hematology,and liver and renal function
tests
The mean general health questionnaire score of exposed was significantly
greater than that of controls.
Exposed had greater overall scores for somatic symptoms,anxiety and
insomnia,but not for personal dysfunction and severe depression
MV Braer – Crum
(1993)
Cross-sectional.
Effect on respiratory tract in children living
close to Braer shipwreck (N = 44 at 3 days
and 56 at 9–12 days after oil spill)
Peak expiratory flow rate
Peak expiratory flow rates were within the normal range in both parts of the
study,and no deterioration was seen over the study period
Sea Empress – Lyons
et al.(1999)
Cross-sectional.
Acute health and psychological effects in
exposed
(N = 539) and controls (N = 550)
Questionnaires of acute symptoms.
HAD and SF-36 scores
Exposed showed significantly higher anxiety and depression scores,worse
mental health and self-reported headache and sore eyes and throat
Sea Empress –
Gallacher et al.
(2007)
Cross-sectional.
Acute symptomathology attributable to
psychological exposure in exposed (N = 794)
and controls
(N = 791)
Questionnaires of acute toxic and non-toxic
symptoms and Hospital Anxiety and
Depression Scale
Perceived risk was associated with raised anxiety and non-toxicologically
related symptom reporting.
Toxic symptom reporting was associated with oil exposure and with raised
perceived risk
Nakhodka – Morita
et al.(1999)
Cross-sectional.
Acute health problems in exposed (N = 282)
Questionnaires of acute and toxic symptoms.
Personal air samplers to assess carcinogenic
benzene,toluene and xylene.
Urine toxicity levels
Levels of hydrocarbons in air were far below the occupational acceptable limit.
The principal complaints of symptoms were low back pain,headache and
symptoms of eyes and throat
Erika – Schvoerer et al.
(2000)
Cross-sectional.
Acute health effects in exposed (N = 3,669)
Questionnaires and telephone interviews on
acute symptoms
The main described acute symptoms were lumbar pain,migraine,dermatitis,
ocular irritation,respiratory problems and nauseas.
Duration of the cleaning work was identified as risk factor
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Table 3.
Continued
Accident – reference
Study characteristics
Methods
Results
Erika – Baars (2002)
Potential toxicological risk assessment for
people involved in cleaning activities and
for tourists
Risk characterizations on the basis of
suppositions of the potential exposure
during cleaning and tourist activities
The risk for the general people was limited.
Increased risk for developing skin irritation and dermatitis,and very limited risk
for developing skin tumors,were described for people who had been in
bare-handed contact with the oil
Erika – Dor et al.
(2003)
Potential toxicological risk assessment after
decontamination of 36 beaches polluted by
the Erika oil spill and seven control beaches
Determination of the 16 PAH selected by the
US EPA in sand,water and surface of rocks.
Seven scenarios of exposure for people using
the beaches were contemplated,and the
most conservative available toxicological
values were selected for computing risks
The sand and water were slightly polluted,with values similar to those found in
the control beaches.The rocky areas were still highly polluted.
No lethal risk was found for a young child who had accidentally ingested a
small ball of fuel.
The life-long excess risks for skin cancer and for all other cancers were about
10-5in scenarios including contact with the polluted rocks.
The hazard quotient for teratogenic effects was very small,except in scenarios
where pregnant women would walk among rocks containing high pollution
levels
Prestige – Suarez et al.
(2005)
Cross-sectional.
Acute health problems among subjects
involved in the cleanup operation after the
spill (N = 800)
Questionnaire on exposure conditions,acute
health problems,and use of protective
material
Bird cleaners accounted for the highest prevalence of injuries.
Working more than 20 days in highly polluted areas was associated with
increased risk of injury in all workers.
Toxic effects were higher among seamen.
No severe disorders were identified
Prestige – Carrasco
et al.(2006)
Cross-sectional.
Association between health information,use
of protective devices and occurrence of
acute health problems in exposed (N = 799)
Questionnaire on exposure conditions,acute
health problems,use of protective material
and health-protection information received
Health-protection briefing was associated with use of protective devices and
clothing.
Uninformed subjects registered a significant excess risk of itchy eyes,nausea/
vomiting/dizziness,headaches and throat and respiratory problems.
Seamen,the most exposed group,were the worst informed and registered the
highest frequency of toxicological problems
Prestige – Zock et al.
(2007)
Longitudinal 12-24 months after the spill.
Association between participation in cleanup
work and respiratory symptoms in exposed
(N = 6780)
Questionnaires with qualitative and
quantitative information on cleanup
activities and respiratory symptoms
The risk of LRTS increased with the number of exposed days,exposed hours per
day,and number of activities.
The excess risk of LRTS decreased when more time had elapsed since last
exposure
Prestige – Carrasco
et al.(2007)
Cross-sectional.
Health-related quality of life and mental health
in residents after 16 months (N = 1350) and
controls
(N = 1350)
Questionnaires of perceived social support
and mental health SF-36,GHQ-28,HADS and
GADS
The SF-36 showed coastal residents as having a lower likelihood of registering
suboptimal values in physical functioning and bodily pain,and a higher
frequency of suboptimal scores in mental health
Prestige – Sabucedo
et al.(2009)
Cross-sectional.
Psychological impact in subjects from 23
coastal locations from three zones according
to their proximity to the location of the spill
(N = 938).
Questionnaires on perceived involvement and
social support,satisfaction with the financial
aid received and social relationships.
Modified version of the CRI-ADULT.
Simplified version of the SCL-36
Affected subjects received a good deal of social support and were satisfied
with the economic aid received.
Those affected with high support and satisfaction scores were in a better
situation than those with low scores,and even better than those not affected
Tasman Spirit – Janjua
et al.(2006)
Cross-sectional.
Acute health effects in exposed residents (N =
216) and controls living 2 km (N = 83) and
20 km (N = 101) far from the coastline
Questionnaires on acute health symptoms and
on perception about the role of oil spill in
producing ill health,and anxiousness about
the effect of oil spill on health
Data showed moderate-to-strong associations between the exposed group and
the symptoms.
There was a trend of decreasing symptom-specific prevalence odds ratios with
increase in distance from the spill site
Tasman Spirit –
Khurshid et al.
(2008)
Cross sectional.
Health parameters of people working/living in
the vicinity of an oil-polluted beach (N =
100)
Hydrocarbon/organic content in seawater and
sand samples.
Hematological and biochemical parameters.
Liver and renal function tests
Seawater had no traces of hydrocarbon content.
Lymphocyte and eosinophil levels were slightly increased.
About 11 people had raised SGPT,but this was not significant
Tasman Spirit – Meo
et al.(2008)
Cross sectional.
Lung function in exposed (N = 20) and
controls
(N = 31)
Spirometry
Significant reduction in FVC,FEV1,FEF25–75%and MVV in exposed.
Lung function parameters were improved when the subjects were withdrawn
from polluted air environment
CES-D, Center for Epidemiologic Studies – Depression; CRI-ADULT, coping response inventory; DIS, diagnostic interview schedule; FEF25–75%, forced expiratory flow; FEV1, forced expiratory volume in first second; FVC, forced vital
capacity; GADS, Goldberg anxiety and depression scale; GHQ, general health questionnaire; HADS, hospital anxiety depression scale; LRTS, low respiratory tract symptomathology; MVV, maximum voluntary ventilation; PAH,
polycyclic aromatic hydrocarbons; PTSD, post-traumatic stress disorder; SGPT, serum glutamic pyruvic transaminase.
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95% CI 1.19–2.92). The mean general health questionnaire score
of the exposed subjects was significantly greater than that of the
controls. The high rate of non-responders among individuals
selected to participate in this study was reported (59 of the 215
non-responders in the first phase of the study and 16 of the 86
non-responders in the second phase were surveyed). The main
reasons for non-responding was not feeling that their health had
been affected, not interested in the study or did not think the
study was useful (Foster et al., 1995).
Crum (1993) performed a cross-sectional study evaluating the
peak expiratory flow rate in two groups of children aged 5–12
years who were resident within 5 km of the Braer shipwreck. The
first measure was carried out three days after the accident in 44
children, and a second one in 56 children between 9 and 12 days
after the oil spill. The main results showed that the children’s
peak expiratory flow rates were within the normal range in both
parts of the study, and no deterioration was seen over the study
period,eveninthechildrenknowntohaveasthma.Nosignificant
difference was observed between the two sets of values (P =
0.502, Student’s t test for paired samples).
Sea Empress
In the wake of the Sea Empress oil spill, Lyons et al. (1999) inves-
tigated the acute health effects (self-reported physical and psy-
chological symptoms) in the residents of the vicinities of the
affected area (Milford Haven, southwest Wales). They designed a
retrospective cohort study that included 539 exposed and 550
controls. Results obtained, after adjustment by age, sex and
smoking status, allowed the conclusion that the people living in
the exposed areas presented high levels of anxiety and depres-
sion scores, worse mental health and self-reported headache
(odds ratio = 2.35, 95% CI 1.56–3.55), sore eyes (odds ratio = 1.96,
95% CI 1.06–3.62) and sore throat (odds ratio = 1.70, 95% CI
1.12–2.60). These last three symptoms were expected from the
known toxicological effects of oil, so the authors suggested a
direct health effect in the exposed population.
On the basis that exposure to a complex emergency has a
substantial psychological component, Gallacher et al. (2007) per-
formed work in 794 exposed individuals and 791 controls in
which anxiety, depression and symptom reporting were used as
measures of the health impact. The main results indicated that
perceived risk was associated with raised anxiety and non-
toxicologicallyrelatedsymptomreporting(oddsratio=2.28,95%
CI 1.57–3.31, P < 0.001), whereas physical exposure to oil was
only associated with toxicologically related symptom reporting.
The authors concluded that psychological exposure was a sub-
stantially more sensitive measure of health impact than physical
exposure in relation to psychological outcomes.
Nakhodka
Moritaet al.(1999),asaresultoftheNakhodkaoilspill,conducted
a study in 282 people (men and women) who joined in cleanup
work. Interviews on health status and determinations of several
hydrocarbon metabolites in urine were carried out. Their results
were similar to those from Campbell et al. (1993), showing that
people suffered mainly from pains in the lumbar region and legs,
headaches and irritation of eyes and throat. The multivariate
logistic regression model was applied to clarify the risk factors of
having at least one symptom with several relevant variables.
Results showed that being of female gender, the number of
working days on cleanup activities, direct exposure to oil and
history of hypertension and low back pain were significant risk
factors for the development of symptoms (P < 0.05). In the urine
analyses, only three individuals showed higher levels of hippuric
acid (>1.0 g l-1) that had returned to normality four months later.
In this study the use of personal air samplers by the cleanup
workers was remarkable. They allowed the determination of the
concentrations of carcinogenic benzene, toluene and xylene in
the environmental air, and their results showed that these levels
were lower than the occupational acceptable limits (10 ppm for
benzene, 100 ppm for toluene and 100 ppm for xylene). The
highest concentration of suspended particles on any given day
was 0.088 mg m-3, also below the occupational acceptable limit
(2 mg m-3).
Erika
Schvoerer et al. (2000) presented a cross-sectional investigation
onhumanhealthriskassessmentasaresultoftheErikaoilspillin
3669 interviewed people, who included cleaning workers and
volunteers. Their results indicated that 7.5% of the individuals
experiencedsometypeofwoundand53%somehealthproblem
(30% lumbar pain, 22% migraine, 16% dermatitis).They reported
in a smaller degree ocular irritation (9%), respiratory problems
(7%) and nausea (6%). The duration of the cleaning work was
identified as a risk factor.
Baars (2002) evaluated the health risk for people involved in
the cleaning activities after the Erika oil spill and also for tourists,
withanemphasisonthecarcinogenicpropertiesoftheoil,onthe
basisoftheknowntoxicologicalpropertiesoftheoilcomponents
and assumptions on the levels of exposure during the perfor-
mance of different activities. In assessing toxic risks the actual
exposure levels were compared with limit values taken from the
literature; in assessing carcinogenic risk the actual exposure
levels were compared with the 1:104lifetime excess risk of devel-
oping tumors. The outcome indicated that the risks for the
general population were limited. For people who had been in
bare-handed contact with the oil there was increased risk of
developing skin irritation and dermatitis, but these effects were
in general reversible, and also that of developing skin tumors,
which was very limited due to the short contact time with the oil.
Dor et al. (2003) reported an assessment of human health risk
after decontamination of beaches polluted by the Erika oil. They
determined the 16 PAH selected by the US EPA in samples of
sand, water and the surface of rocks from 36 cleaned-polluted
beaches and seven control beaches, and contemplated seven
possible scenarios of exposure for people using the beaches in
tourist activities (children, adults and pregnant women) or
working activities. The life-long excess risk for skin cancer and
forallothercancerswasabout10-5inscenariosincludingcontact
with the polluted rocks. The authors concluded that exposure
was mainly associated with polluted water among children and
with contaminated rocks for adults, and that, despite uncertain-
ties, decontaminated beaches did not entail any significant
health risks and could be opened to the public.
Prestige
As a result of the disaster of the tanker Prestige, densely popu-
latedcoastalregionsofSpain(Galicia,Asturias,Cantabriaandthe
Basque country), as well as the neighboring French coasts, with
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intense activity of extraction of marine resources and tourism,
were affected. Several studies were performed after this accident
in order to evaluate the possible human health effects.
Suarez et al. (2005) evaluated the conditions of exposure and
the acute health effects in individuals who participated in the
cleanup works in the regions of Asturias and Cantabria (Spain),
and the association between these and the type of work. Four
hundred individuals from each region were interviewed. Col-
lected data included information on the work performed, use of
protectiondevicesandacutesymptoms.Birdcleanersaccounted
for the highest prevalence of lesions (19%, P < 0.001), including
neurovegetative disorders (11.2%, P = 0.169) and low back pain
(3.1%, P = 0.281). Working periods longer than 20 days in highly
polluted areas were associated with increased risk of injury in all
workers. A specific analysis restricted to seamen only found a
strong and significant association with having worked for more
than 3 days (odds ratio = 14.30 and 11.02 for categories of 3–20
days and over 20 days, respectively) and having torn or not worn
the protective suit (odds ratio = 1.20 and 7.79, respectively), but
no severe disorders were identified among individuals analyzed.
The same authors reported another study examining the asso-
ciation between use of protective devices, frequency of acute
health problems and health-protection information received by
799 exposed individuals, classified according to the tasks per-
formed (Carrasco et al., 2006). These authors observed a signifi-
cantexcessriskofitchyeyes(oddsratio=2.89;95%CI1.21–6.90),
nausea/vomiting/dizziness (odds ratio = 2.25; 95% CI 1.17–4.32)
and throat and respiratory problems (odds ratio = 2.30; 95% CI
1.15–4.61) among uninformed subjects. Furthermore, there was
a noteworthy significant excess risk of headaches (odds ratio =
3.86; 95% CI 1.74–8.54) and respiratory problems (odds ratio =
2.43; 95% CI 1.02–5.79) among uninformed paid workers.
Seamen, the group most exposed to the spilled oil, were the
worst informed and registered the highest frequency of toxico-
logical problems. Therefore, the authors confirmed the results
obtained in their previous study and found a significant associa-
tion between proper health-protection briefing and use of pro-
tective devices and lower frequency of health problems.
Zocket al.(2007)evaluatedtheprevalenceoflowerrespiratory
tract symptoms (LRTS) more than a year after Prestige accident in
6780 fishermen who had participated in the cleanup labors
(response rate 76%), through questionnaires that included quali-
tative and quantitative information. Their results showed that
LRTS was more prevalent in cleanup workers (odds ratio = 1.73;
95% CI 1.54–1.94), and that the risk of LRTS increased in relation
to the number of exposed days, exposed hours per day and
number of activities carried out (linear trend, P < 0.0001). The
excess risk of LRTS decreased with elapsed time since last expo-
sure (odds ratio = 2.33, 1.69 and 1.24 for less than 14 months,
14–20months,andmorethan20months,respectively),although
it was still significant when more than 20 months had elapsed.
Carrasco et al. (2007) performed a new study on the effects of
the Prestige oil spill on health-related quality of life (HRQoL) and
mental health in the affected population, approximately 18
monthsafterthisdisaster,usingseveralquestionnaires. Themain
results showed coastal residents as having a lower likelihood of
registering suboptimal HRQoL values in physical functioning
(odds ratio = 0.69; 95% CI 0.54–0.89) and bodily pain (odds
ratio = 0.74; 95% CI 0.62–0.91), and a higher frequency of subop-
timal scores in mental health (odds ratio = 1.28; 95% CI 1.02–
1.58). The authors concluded that, almost one and a half years
after the accident, worse HRQoL and mental health levels were
not in evidence among subjects exposed to the spilled oil. Nev-
ertheless, a slight impact on the mental health of residents in the
affected areas was suggested by some of the scales applied.
Similar results were obtained by Sabucedo et al. (2009), who
evaluated the psychological impact of Prestige oil spill. They
carried out a descriptive study that involved 938 men and
women from 23 localities throughout the Galician coast. Half of
them were fishermen or workers related to the extraction of
fishing resources, and the other half were not linked to these
activities. Questionnaires on different psychological and psycho-
social factors were filled in at the time of the accident and one
year after. The results showed that the affected subjects had
receivedagooddealofsocialsupportandweresatisfiedwiththe
economicaidreceived.Inaddition,affectedindividualswithhigh
support and satisfaction scores were currently in a better situa-
tion than those affected with low scores, and even better than
those not affected.
Tasman Spirit
Janjua et al. (2006), following the Tasman Spirit shipwreck, con-
ducted a study which included an exposed group composed of
adults of both genders living on the affected coastline (N = 216)
and two control groups living 2 km (N = 83) and 20 km (N =101),
respectively, away from the indicated area. Surveys on acute
symptoms related to eyes, respiratory tract, skin and nervous
system, aswellasconsultationsofallergies,tobaccoconsumption
and perceptions on the effect on their health and anxiety about
their health effects were performed. Their results showed
moderate-to-strongassociations(prevalenceoddsratiosranging
from2.3to37.0)betweentheexposedgroupandthesymptoms,
whichdecreasedwiththedistancefromthespillsite, andmultiple
linear regression model revealed strong relationship of exposure
status with the symptoms score (b = 8.24, 95% CI 6.37–10.12).
Khurshid et al. (2008) presented a short-term study in people
who were working or living in the vicinity of Karachi beach.
Hematological and biochemical parameters were determined,
andliverandrenalfunctiontestswerecarriedout.Theyalsotook
seawater and sand samples and analyzed them for hydrocarbon/
organiccontents.Theresultsonlyshowedslightrisesinthelevels
of lymphocytes and eosinophiles. The authors recommended
performing follow-up studies after oil spills taking samples every
3 months for 3–5 years, noting respiratory disorders and any
changes in the skin.
Finally, Meo et al. (2008) assessed, by means of spirometry,
lung function and followed up the progression after one year in
20 subjects exposed to this oil spill and 31 controls. Subjects
exposed to polluted air had significant reductions in lung func-
tioncomparedwiththeirmatchedcontrols(Prangingfrom0.001
to 0.02 for the different lung function parameters). The reported
impairment was reversible and lung function parameters were
improved when the subjects were withdrawn from the polluted
air environment.
In summary, studies performed after Exxon Valdez spill only
accounted for psychological effects in the exposed populations.
For all the other accidents, there are also studies on acute toxic
effects,andmoreover,fortheErikaoilspilltherearetwoworkson
potential toxicological risk assessment, both concluding that
exposure to pollutants contained in the oil during common
activities did not entail any significant health risk. Data obtained
in most of these studies indicated that technological disasters
that involve oil spills have acute physical consequences
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that diminish with time and are mainly reversible, and psycho-
logical consequences and continuing disruptive and stress-
provoking consequences for resident communities. The results
also suggested that conflicting definitions of long-term effects
and recovery of the natural environment contributed to commu-
nity stress.
EPIDEMIOLOGICAL STUDIES ON
GENOTOXICITY AND ENDOCRINE TOXICITY
Table 4 displays a summary of the main characteristics of these
studies.
Braer
Cole et al. (1997) evaluated the possible genotoxicity as a conse-
quence of the Braer tanker oil spill. They used blood samples to
assess the primary damage in the DNA (DNA adducts in the
mononuclearcellfractionbyamodified32P-postlabelingmethod
andmutationsatthehprtlocusinTlymphocytes). Theseauthors
did not obtain any evidence of genotoxicity for either end point,
but they proposed several issues to be taken into account in the
design of biomonitoring studies after oil spills.
Prestige
Laffon et al. (2006) conducted a study to determine the possible
genotoxicdamageassociatedwiththeexposuretoPrestigeoil,in
34 volunteers, who worked in autopsies and cleaning of oil-
contaminated birds, and 35 controls. Environmental concentra-
tions of volatile organic compounds (VOC) in the working room
were determined. Genotoxicity was evaluated by means of
micronucleus (MN) test and comet assay, and the possible influ-
ence of several DNA repair genetic polymorphisms was also ana-
lyzed.Their results showed significantly higher DNA damage (P <
0.01), but not cytogenetic damage, in relation to the exposure
time (r = 0.376, P < 0.05), and also certain exposure–genotype
interactions.
Pérez-Cadahía and colleagues performed a study with the
objective of evaluating the genotoxicity and endocrine toxicity
related to exposure to Prestige oil during the different cleaning
labors. Exposed individuals were classified into three groups:
manual volunteers, hired manual workers and hired workers
using high-pressure water machines. The environmental expo-
sure levels of VOC were determined, and different biological
parameters were measured. Their results were published in dif-
ferentpapers.Inaninitialstage(Pérez-Cadahíaet al.,2006,2007),
arelativelysmallpopulation(68totalexposedvs42controls)was
analyzed. The data obtained indicated that the highest levels of
VOCwereobservedinthevolunteerenvironmentandthatexpo-
sure to Prestige oil induced genotoxic damage (tests applied:
sister chromatid exchanges (SCE), MN test and comet assay), the
comet assay being the most sensitive test to detect it, and alter-
ations in hormonal status (prolactin and cortisol plasma concen-
trations, significant decreases with P < 0.01). Also, gender, age
and tobacco smoking influenced the levels of genetic damage,
while the effect of using protective devices (clothes and mask)
was less noticeable than expected.
Later, they enlarged the study with the aim of checking the
validity of their previous data, including 180 exposed subjects
and 60 controls. Their results showed significant increases in the
levels of blood heavy metals (aluminum, nickel and lead) and
DNA damage, and alterations in the endocrine status of the
exposed populations (significantly higher prolactin plasma con-
centrations,P<0.01;Pérez-Cadahíaet al.,2008a).Theyalsofound
generalincreasesinMNfrequencyanddecreasesintheprolifera-
tionindexintheindividualswithlongertimesofexposure(Pérez-
Cadahía et al., 2008b). Moreover, significant influence of several
geneticpolymorphismsinmetabolizingenzymesandDNArepair
proteins was observed. In addition, their previous results
showing the absence of effect of using protective devices were
confirmed.
Finally, the same authors (Pérez-Cadahía et al., 2008c) investi-
gated the relationship between blood levels of heavy metals and
genotoxic or endocrine parameters in the individuals exposed to
Prestige oil. Cortisol plasma concentration appeared to be the
mostsensitiveparametertotheeffectsofmetalexposure,sinceit
was significantly influenced by blood concentrations of alumi-
num,nickel(bothinversely)andcadmium(positively),andjointly
by aluminum and nickel. On this basis, the authors suggested
plasma levels of cortisol as a potentially relevant biomarker to
assess the effects of exposure to heavy metals.
Taking into account the known genotoxic, cancer-provoking
and endocrine disrupting properties of many compounds con-
tained in the spilled oils, it seems surprising that only for two oil
spills (Braer and Prestige) are there studies contemplating these
consequences for human health in exposed individuals. The
results obtained in most of these studies provide evidence of
genotoxicityandalterationsinthehormonalstatusrelatedtothe
exposure. The only work with negative results (Cole et al., 1997)
comprised a relatively small population (26 exposed vs 9 con-
trols), and nothing is specified on the participation of the
exposed individuals in the cleanup tasks; only their status as resi-
dents in the polluted area is mentioned. It seems probable that
direct participation in the cleanup work involved a higher expo-
sure to the oil toxic compounds than that experienced by zone
inhabitants who did not participate in the cleaning.
CONCLUSIONS
Untilnowtherehavebeen38largeoilspills,butonlyforsevenof
themhavestudiesontherepercussionsoftheexposuretospilled
oils on human health been performed. Most of these investiga-
tions correspond to cross-sectional epidemiological studies that
analyze acute physical effects or psychological consequences in
the affected people. Some of them do not include a matched
control population, which makes the information provided con-
fusing and difficult to interpret. A smaller number of studies are
in vitro or in vivo approaches aiming to investigate the effects at
thecellularlevelandtheabilityoftheoilcompoundstobetrans-
ferred into the food chain and induce damage in consumers;
others are focused on biological markers indicative of genotoxi-
city and/or endocrine toxicity.
On the occasion of the Prestige oil spill, Porta and Castaño-
Vinyals (2003) recommended
studies of exposure to the spilled oil on the medium- and long-
term impact on human health. In addition to a first transversal
stage, they recommend the monitoring of the exposed popula-
tions in a second longitudinal stage. This would allow (i) deter-
mination of whether the biomarkers of internal dose, of
biologically effective dose and of early biological response
performing epidemiological
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Table 4.
Epidemiological studies on genotoxicity and endocrine toxicity (ordered by the chronology of the spills)
Accident – reference
Study characteristics
Methods
Results
Braer – Cole et al.
(1997)
Longitudinal.
Genotoxicity in residents (N = 26) and controls (N = 9)
at 3 sampling times (10 days,10 weeks and 1 yearafter the accident)
DNA adducts in the mononuclear cell fraction and fre-
quency of hprt mutations in T lymphocytes
No evidence of genotoxicity was obtained for either
end point
Prestige – Laffon et al.
(2006)
Cross-sectional.
Genotoxicity in individuals performing autopsies and
cleaning of oil-contaminated birds (N = 34) and con-
trols (N = 35)
Environmental VOC.
Comet assay and MN test.DNA repair genetic polymor-
phisms (XRCC1,XRCC3,APE1)
Significant increase in the comet assay,but not in the
MN test,related to the time of exposure.
Exposed individuals carrying XRCC1-399Gln or APE1-
148Glu alleles showed increased DNA damage
Prestige – Pérez-
Cadahía et al.(2006)
Cross-sectional.
Genotoxicity in volunteers and hired workers partici-
pating in the cleanup (N = 68) and controls (N = 42)
Environmental VOC.
Comet assay,SCE,MN test
Highest VOC levels in the volunteer’s environment.
Significant increase in the comet assay in exposed indi-
viduals.
Influence of sex,age and tobacco smoking on the
genotoxicity variables.
No effect of using protective mask during cleanup
labors
Prestige – Pérez-
Cadahía et al.(2007)
Cross-sectional.
Gentoxicity and endocrine alterations in volunteers
and hired workers participating in the cleanup (N =
68) and controls (N = 42)
Environmental VOC.
Heavy metals in blood (Al,Cd,Ni,Pb,Zn).
SCE.
Prolactin and cortisol.
Metabolic genetic polymorphisms (GSTM1,GSTT1,
GSTP1)
Highest VOC levels in the volunteer’s environment.
Significant increase in the levels of Al,Ni and Pb,and
decrease of Zn,in exposed individuals.
Significant increase in SCE rate in exposed,influenced
by age,sex,smoking and GSTM1 polymorphism.
Significant decrease in prolactin and cortisol levels in
exposed subjects
Prestige – Pérez-
Cadahía et al.
(2008a)
Cross-sectional.
Gentoxicity and endocrine alterations in volunteers
and hired workers participating in the cleanup (N =
180) and controls (N = 60)
Heavy metals in blood (Al,Cd,Ni,Pb,Zn).
Comet assay.
Prolactin and cortisol.
Metabolic genetic polymorphisms (CYP 1A1,EPHX1,
GSTM1,GSTT1,GSTP1)
Significant increase in the levels of Al,Ni and Pb,and
decrease of Zn,in exposed individuals.
Significant increase in comet assay and decrease in
cortisol levels in exposed individuals.
Higher DNA damage was related to CYP 1A1 and
EPHX1 variant alleles,and lower DNA damage to
GSTM1 and GSTT1 null genotypes
Prestige – Pérez-
Cadahía et al.
(2008b)
Cross-sectional.
Gentoxicity in volunteers and hired workers participat-
ing in the cleanup (N = 159) and controls (N = 60)
MN test. Metabolic genetic polymorphisms (CYP 1A1,CYP 1B1,
EPHX1,GSTM1,GSTT1,GSTP1).
DNA repair genetic polymorphisms (XRCC1,XRCC3,
XPD)
General increases in MN frequency and decreases in
the proliferation index were observed in individuals
with longer time of exposure.
All the polymorphisms analyzed,excepting for CYP 1B1
and XRCC1,influenced cytogenetic damage levels
Prestige – Pérez-
Cadahía et al.
(2008c)
Cross-sectional.
Relationship between blood concentrations of heavy
metals and cytogenetic and endocrine parameters in
exposed by means of univariate statistics (general
linear model) (N = 179).
Heavy metals in blood (Al,Cd,Ni,Pb,Zn).
Comet assay,SCE,MN test.
Prolactin and cortisol
Pb was related to the comet assay.
Cortisol plasma concentration was influenced by Al
and Ni inversely and by Cd positively.
In women there was a strong association between Cd
and prolactin levels
MN, micronucleus test; SCE, sister chromatid exchanges; VOC, volatile organic compounds.
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remain stable with time or undergo variations; (ii) determination
of certain factors influencing the mentioned biomarkers; and (iii)
analysis of the levels of biomarkers or any other factor associated
with the appearance of a particular illness, subclinical effects or
interesting alterations (physiological, genotoxic, etc.).
Some studies compare the evaluated or estimated exposure
levels with occupational acceptable exposure limits, or use these
limits to calculate the potential toxicological risk. Nevertheless,
this comparison is not entirely correct, since the occupational
limitsareusuallydefinedforexposuresof8 h/dayduringawhole
working life, i.e. considering a chronic exposure. Exposure to
spilled oils takes place over several days or some months at the
most, involving time periods much shorter than occupational
exposures.
In summary, most of the studies collected in this review
provide evidence on the relationship between exposure to
spilled oils and the appearance of acute physical, psychological,
genotoxic and endocrine effects in the exposed individuals. Con-
sideringtherelativelyhighfrequencyofthiskindofenvironmen-
tal disaster, it seems necessary to establish detailed intervention
protocols that include some mechanisms to detect and control
the possible harmful health effects that exposure can induce,
including performing the immediate collection of biological
samples from the beginning of the cleanup work, in order to
establish the levels of individual internal exposure effects at the
acute and chronic level, especially those related to genotoxicity.
This will permit not only determination of the risk that exposure
may involve, but also evaluation of whether protective devices
used by the individuals in each case adequately fulfilled their
function, or on the contrary they did not exert the required pro-
tection and therefore require to revision of material characteris-
tics and improved briefing sessions on their correct use.
Acknowledgments
This work was funded by a grant from the Xunta de Galicia
(INCITE08PXIB106155PR). F. Aguilera was supported by a fellow-
ship from the Fundación Carolina.
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